Leaf Induction Impacts Behavior and Performance of a Pollinating Herbivore

Abstract

Flowering plants use volatiles to attract pollinators while deterring herbivores. Vegetative and floral traits may interact to affect insect behavior. Pollinator behavior is most likely influenced by leaf traits when larval stages interact with plants in different ways than adult stages, such as when larvae are leaf herbivores but adult moths visit flowers as pollinators. Here, we determine how leaf induction and corresponding volatile differences in induced plants influence behavior in adult moths and whether these preferences align with larval performance. We manipulated vegetative induction in four Nicotiana species. Using paired induced and control plants of the same species with standardized artificial flowers, we measured foraging and oviposition choices by their ecologically and economically important herbivore/pollinator, Manduca sexta. In parallel, we measured growth rates of M. sexta larvae fed leaves from control or induced plants to determine if this was consistent with female oviposition preference. Lastly, we used plant headspace collections and gas chromatography to quantify volatile compounds from both induced and control leaves to link changes in plant chemistry with moth behavior. In the absence of floral chemical cues, vegetative defensive status influenced adult moth foraging preference from artificial flowers in one species (N. excelsior), where females nectared from induced plants more often than control plants. Plant vegetative resistance consistently influenced oviposition choice such that moths deposited more eggs on control plants than on induced plants of all four species. This oviposition preference for control plants aligned with higher larval growth rates on control leaves compared with induced leaves. Control and induced plants of each species had similar leaf volatile profiles, but induced plants had higher emission levels. Leaves of N. excelsior produced the most volatile compounds, including some inducible compounds typically associated with floral scent. We demonstrate that vegetative plant defensive volatiles play a role in host plant selection and that insects assess information from leaves differently when choosing between nectaring and oviposition locations. These results underscore the complex interactions between plants, their pollinators, and herbivores.

Mutualism has its limits: consequences of asymmetric interactions between a well-defended plant and its herbivorous pollinator

“…Instead, we observed constitutive emissions of such compounds from Lin− O. harringtonii plants at significantly greater rates than those from Lin+ plants (figure 4a,c), but no evidence for induced increases in VOC emissions from Lin− plants during or after herbivory (figure 4b,d). Our randomized location of these plants in the greenhouse, combined with our recent measurement of the expected volatile responses in four Nicotiana species using the same methods [59] lends confidence to these conclusions. Similarly, the demonstration that leaf herbivory induces JA and phenolic accumulation in flower buds (but not seeds) of Oenothera biennis, with concomitant reduction of damage by moth larvae that eat buds (but not those that eat seeds) [57], suggested a mechanism for reduced performance of H. lineata larvae on living O. harringtonii plants (figure 3c).…”

“…Instead, we observed constitutive emissions of such compounds from Lin− O. harringtonii plants at significantly greater rates than those from Lin+ plants (figure 4 a,c ), but no evidence for induced increases in VOC emissions from Lin− plants during or after herbivory (figure 4 b,d ). Our randomized location of these plants in the greenhouse, combined with our recent measurement of the expected volatile responses in four Nicotiana species using the same methods [59] lends confidence to these conclusions.…”

“…Flowering O. harringtonii plants were innately attractive to adult H. lineata as nectar sources and oviposition sites (figures 1 and 2) but were poor hosts for the larvae, which showed low growth and high mortality at all experimental scales (figure 3; electronic supplementary material, figure S2). Oviposition preferences appeared to adaptively track patterns of larval growth and survivorship in binary choice assays between Lin+ and Lin− plants (figure 2; see [59]), but moths without alternatives (no-choice assays) laid nearly as many eggs (190–220 per night) on these poor hosts as they did on Mirabilis jalapa (225–245 per night), a demonstrably better host (data not shown). Robust resistance of O. harringtonii plants against herbivory by H. lineata appears to be constitutive (figures 4 and 5), suggesting that moth populations are subsidized by other plant species as larval hosts, either within the local shortgrass prairie habitat [60] or in adjacent regions, from which the moths may disperse [61].…”

Mutagenesis of Odorant Receptor Coreceptor Orco Reveals the Odorant-Detected Behavior of the Predator Eupeodes corollae

“…Olfactory senses play a decisive role in this process. Insects can use a precise olfactory system to distinguish the odorants that attract or inhibit oviposition, so as to locate a suitable oviposition substrate [33,34]. Our study found that the egg-laying numbers of FHo were significantly lower than those of the same mating state FWT, regardless of whether they mate with MWT or MHo, suggesting that the egg-laying decisions of females were altered under conditions where the olfactory system is almost lost (Figure 5A).…”

Dynamic environmental interactions shaped by vegetative plant volatiles

“…Although stress-induced volatiles have been shown to deter foliar oviposition by tobacco hornworm ( Manduca sexta ) adults on tobacco plants, the same volatiles were also shown to attract foraging M. sexta adults to flowers and thus enhance pollination. 212 In agarwood ( Aquilaria sinensis ), GLVs released from seeds can attract Vespa hornets, which are important seed dispersers. Additionally, many of these volatiles are similar to those induced during foliar herbivory; this has been suggested to be a repurposing of plant defense to facilitate effective seed dispersal.…”